ADAPTATIONS OF HORNED LARKS (EREMOPHILA
ALPESTRIS) TO HOT ENVIRONMENTS
CHARLES
H.
TROST
THE adaptations of similar animals to different environments are of
particularevolutionaryinterest. Only a few of the many studiesof the
adjustmentsof vertebrates to rigorous environmentshave dealt with
closelyrelatedpopulations(or species)living in contrasting
environments
(Salt, 1952; Dawson,1954; Cade and Bartholomew,1959; Hudsonand
Kimzey, 1966; Brown,1968).
Most small birds are diurnal, and therefore are often exposedto extremesof heat and associatedproblemsof temperatureregulation. Consequently a bird may live in an entirely different microclimatethan a small
nocturnalmammal with which it is sympatric. The Horned Lark (Eremophilaalpestris)is an excellentsubjectfor study. It is ground-dwelling,
diurnal, small (25-40 g), and occupiesopen country with low or sparse
vegetation. It nestsin grasslands,
arctic and alpine tundra, salt marshes,
and deserts. Suchexposedhabitats offer the lark little protection.
HornedLarks belongto an Old World family, Alaudidae,of whichthey
are theonlyindigenous
New Worldrepresentative.
They are foundthroughout the Holarctic and an isolatedpopulationlives in Colombia. Of the
40 subspecies
of Horned Larks recognized,14 are in the Old World and
26 in the New (Peters, 1960).
This study of behavioraland physiologicaladaptationsof two subspeciesof Horned Larks undertakesto comparean inland valley form
from a relativelyrnesicenvironment(E. a. actia) with a desertform
(E. a. ammophila). The environmentsin which these subspecieslive
differ especiallywith respectto temperature,humidity, and available
water.
The inland valley form (actia), hereaftercalledthe mesicform, is the
more widespreadof the two subspecies,
occurringfrom northernCalifornia
(Humboldt County) southalong the entire westernhalf of California to
northernBaja California (30ø N). This race occursin many different
habitats,and Behle (1942) pointsout that it is outstandingin its range
of ecologicaltolerances.At various points along the periphery of its
range it intergradeswith five other subspecies.Also as this race is nonmigratory, individualsare subjectedto the environmentalinfluencesin
the samelocalitythe year around. In correlationwith thesefactors,this
race is the most variable in color of the eight California subspecies.The
leastvariableandmosttypicalrepresentatives
are foundfromLosAngeles
to SanDiego (Behle, 1942).
506
The Auk, 89: 506-527. July 1972
July 1972]
Horned Lark Adaptations to Heat
507
The desert lark (ammophila) occurs sporadically in the level areas
and valleysof the entire Mojave Desert. The altitude of the desertfloor
varies from 700 m near Palmdale,to about 1,500 m in the Owen'sValley.
The climate is hot in the summer(30 ø to 50øC) and cold in the winter
(-10 ø to 20øC), with low rainfall and humidity (Jepson, 1925). The
predominantplant over much of this lark's range is creosotebush (Larrea
tridentata), which providesmore shadethan is presentin the habitat of
most of the other races. This lark is also nonmigratory,and variation between individualsis almost as pronouncedas that in actia, with which
it intergrades in the southwesterncorner of the San Joaquin Valley
(Behle, 1942).
M^TERmLS
^•D
MET•rODS
Capture and maintenance.--A total of 30 actia and 27 ammophila were used in
this study. All were caught in 18-m, sand-colored m!st nets. Usually several nets
were placed in a row. As the Horned Lark subspeciesare very similar in appearance,
no attempt was made to capture larks in the large, mixed wintering flocks. Instead,
all birds were taken on the breeding grounds during the nesting season. The actia
specimenswere caught in a large pasture 5 km west of Warner Springs,San Diego
County, California, at an elevation of about 975 m; the ammophila came from the
AntelopeValley, Los AngelesCounty, California, about 40 km northwest of Lancaster
at about 800 m.
After capture the larks were banded with individual colored leg bands, taken to
the campusof the Univtersity of California at Los Angeles,and placed in large outdoor flight cages. Larks are gregariousbirds, so keeping large numbers together in
the flight cageswas not difficult. At least a week before they were to be measured,
the larks were taken into the laboratory and maintained in a windowless,ventilated
room with a controlled photoperiod (lights on from 09:00 to 21:00). The ambient
temperature in the room remained constant at about 23øC in the winter and 25øC
in the summer. The relative humidity in the room varied between40 and 60 percent.
The larks were housed in individual Hendrix bird cages measuring 26 X 26 X 24
cm. Paper covered the floor and a small rock in the middle gave the lark a place to
stand. Water was provided from inverted 100-ml graduated cylinders, fitted with a
stopper and an L-shaped drinking tube inserted through the bars in the cage. The
birds were fed a commercial assortment of small bird seedsthroughout the study.
Metabolic measurements.--Oxygen consumption was measured in an open flow
system using a Beckman G-2 oxygen analyzer coupled to a recording potentiometer
that recorded the percent oxygen in the air at consecutive 5-minute intervals from
two animal chambersand a blank. The chamberswere made from 3.8-1 (1 U.S.
gal) jars in which a platform of wire mesh (0.6 cm2) was inserted over a layer of
mineral oil to collect urine and feces. The lids were fitted with ports for the passage
of air into and out of the chamber, and for a thermocouple connectedto a Brown
strip chart potentiometer for recording ambient temperature (T_•). One of the l•ds
also had a port for a humidity probe which led to an Aminco electric hygrometer,
and allowed a continuous record of humidity. The air was dried with silica gel
and indicating drierite (CaSO4) before being metered to the chambers. The effluent
air was redried in a U-tube of drierite and then passedto the analyzer. Evaporative
water loss was determined gravimetrically after passing expired air through the
previously weighed Uqtube for 30 minutes. The flow rate was regulated at 700
508
C•r^m.•s H. TROST
Horned Lark
[Auk, Vol. 89
O2 Consumption
y:5.32
- .09X
Day
•
•6
........
f
/
Z.
5
10
15
20
25
.... /
30
35
40
45
TA øC
Figure 1. The relation of oxygen consumption to ambient temperature (T•O.
The vertical lines represent the ranges; horizontal lines, mean values; rectangles,95
percent confidenceintervals (X ñ tSE). The numbers are the number of different
birds in each sample. The comparative measurements on this and remaining figures
were taken at 5ø intervals, starting with 5øC, but were displacedfor graphic purposes. The equations are for lines fitted to the data by the method of least squares.
Both subspecies
are included in the figure.
cc/min at Tx's of 5ø to 40øC. At 45øC the flow rate was increasedto 1,500 cc/min
in order to maintain a low chamber humidity. Tx was regulated within ñ 0.5øC
by placing the animal chambers in a controlled temperature box. Minimal oxygen
consumption was determined by averaging the lowest two 5-minute readings after
the bird had been in the chamber at a given Tx for at least an hour. Except for the
24-hour runs all daytime and nocturnal measurementswere made on postabsorptive
birds in the dark, and the oxygenconsumptionwas correctedto standard temperature
and pressure.Body temperature(T•) was measuredat the end of eachmetabolic
run by inserting a quick-registering mercury thermometer at least 2 cm into the
cloaca. Data from both subspecieswere lumped for most of the measurements,
and separatedonly for specialconsideration.
Water consuraption.--In measurements of ad libitura water consumption the
fluid intake and body weight were recordeddaily before the lights came on (09:00).
The windowlessbird room was used for measurementsat T.• ---- 23øC, and a ModuLab, walk in, controlledtemperaturecabinet was used for T,• --• 33øC. The relative
humidities varied between 40 and 60 percent at 23øC, and 24 and 39 percent at
33øC. In all cases an extra drinking device was used to correct for evaporation.
July 1972]
HornedLark Adaptationsto Heat
509
Horned
Lark
%,,.••..•octurna
02
Consump
•
:T^ 11øC
...........
1• 20øC
2'1 '
' o'1 ' &
'
'
' o½ '
Time of Day
Figure 2. Decreasein oxygenconsumptionat night in four desert Horned Larks
(E. a. ammophila)at two ambienttemperatures.The dark period is indicatedby
the black bar between 21:00 and 09:00.
Minimal water consumption
was determinedby reducingthe quantity of water daily
until a level was reachedbelowwhichthe animalscouldno longermaintainweight.
RESULTS
Oxygenconsumption.--Oxygen
consumption
was inverselyrelated to
ambienttemperaturebelow 35øC (Figure 1). During the daytime
thermal neutrality was at about 35øC, whereasat night the thermal
neutral zone extendedto below 25øC. At any given temperaturethe
oxygenconsumption
was lower at night than during the day. The minimum oxygenconsumption
of 2.28 cc O2/g/hr was about 25 percentlower
thanthat predictedby the equationof Lasiewskiand Dawson(1967) for
a passerine bird of this size. Between 35ø and 40øC the increase in
oxygenconsumption
was accompanied
by an increasein TB (41.0ø and
42.5øC,respectively),
and had a Q•oof 2.0. At 45øC the meanoxygen
consumption
increased
furtherto 3.38 cc O2/g/hr, with a Q•oof 3.1 (T,
increased
from42.5ø to 45.0øC).
At night the metabolism
of the birdsbeganto drop as soonas they
were placed in the darkenedchamber (Figure 2). The lowest rates
CHARLES H.
510
Horned
TROST
[Auk, Vol. 89
Lark Conductance
.5
.4
.3
.2
.1
I
I
I
I
I
I
5
10
15
20
25
30
•
T^øC
Figure 3. The relation of thermal conductance to ambient temperature. Symbols,
numbers,and symbol displacementas in Figure 1.
usually occurredbetween23:00 and 05:00, after which the metabolism
beganto increaseas the birds anticipatedtheir usualphotoperiod(09:00).
Thermalconductance.--Both
the daytimeand nocturnalcurvesof oxygen consumption extrapolated to ambient temperatures above the ob-
served body temperatures,indicating either a change in thermal conductanceor a high metabolismcausedby excitement(Hudson and Kimsey, 1966). The two regressionlines were fitted to the data below thermal
neutrality by the methodof least squaresand each had a correlationcoefficientof 0.9. The slopesof the daytime (0.09) and nocturnal(0.10)
curveswere nearly parallel. The thermal conductance(C) was calculated
from the followingequation:
C = M/TB - TA
where m is the metabolicrate in cc O,g/hr and TB -- TA is the differencebetweenbody and ambient temperaturein øC. Both the daytime
and nocturnal thermal conductanceshad a slope not different from zero
between5ø and 15øC (Figure 3). The mean thermal conductances
were
0.15 and 0.12 cc 02/g/hr/ø C for day and night, respectively.Above 15øC
July 1972]
Horned Lark Adaptations to Heat
Horned
5c
511
Lark
Body Temperature
3
3 D•ay
•-•35
Night
/
,,.,-"•
3C
•
10
15
20
25
30
35
40
45
T^ø½
Figure 4. The relation of body temperature(T B) to ambient temperature(TA).
Symbols, numbers, and symbol displacementas in Figure 1. The dashed line equates
body and ambient temperature.
the thermal conductanceincreasedin a curvilinear fashion for both, and
the nocturnalvalueswere lower than thoseduring the day at all temperatures except30øC.
Body temperature.--Asthe rate of heat productiondecreasedat night
and the thermal conductance remained about the same in low ambient
temperatures,one would expecta lower body temperatureat night (Figure 4). At ambient temperaturesfrom 5ø to 30øC, the mean Tn was 2.0ø
to 2.5øC lower at night than during the day, but at 35øC there was no
difference. At 40ø and 45øC the larks underwenta markedhyperthermia
(mean TB: 42.5ø and 45.0øC, respectively).
Chamber humidity.--The chamber humidity is a result of the amount
of water lost by the bird and the flow rate. The humidities measured
during the metabolicdeterminationsare presentedin Table 1. The absolute humidity during the daytime was constantbetween 5ø and 35øC,
and at 40øC it increasedthreefold. As the flow rate of dry air at 45øC
was doubled over that at 40øC, the humidity at 45øC increasedonly
slightly, while the water output of the birds increasedgreatly. The
chamberhumiditiesat night were lower than those during the day at
512
CIlARLESH. TROST
TABLE
[Auk, Vol. 89
1
ABSOLUTE HUMIDITY •t IN TIlE METABOLIC GItAMBER
5oc
Daytime
Mean (X)
15oc
20øC
25øC
30øC
35øC
40øC
45øC
3.22
3.94
2.74
3.69
2.11
2.08
7.64
8.86
Samplesize (N)
3
4
6
4
7
9
9
8
Standard error of X
0.00
0.27
0.87
1.05
0.46
0.35
1.32
1.21
Night
Mean (X)
1.70
1.23
0.75
1.05
1.88
Samplesize (N)
2
6
3
2
1
0.21
0.06
Standard error of X
•g H.•O/rn a air.
comparabletemperatures,correlatingwith the birds' decreasedwater output at night.
Evaporative water loss.--The daytime evaporative water loss varied
between11 and 15 percentof the body weight per day from 5ø to 35øC
(Figure 5). The water lossat night (7 to 9 percentof the body weight
per day) was lower than during the day at all temperaturesbetween 5ø
Horned
Lork
II
o
,,
Io(
Pulmo-cutan
Water
Loss
/
/
o
2o 6 D_ay 6
•I
5
............
I
10
•I
15
•"
7
,[,
.... '•4
.... -•I
I
20
25
WNight
30
35
40
45
T•øC
Figure 5. The relation of evaporative water loss to ambient temperature. Symbols,numbers,and symboldisplacementas in Figure 1.
July 1972]
Horned Lark Adaptations to Heat
513
Horned Lork
Evaporatio
/Heat
Product
'7
r•o
•
•o
ß1-
60
'
5
'
I0
'
15
'
'
20
25
'
30
T• oC
Figure 6. The ratio of heat produced to heat lost by evaporation in relation to
ambient temperature. Symbo• and numbers as in Fibre 1. The dashed line is indicative of the level at which 1• percentof the heat produced• lost by evaporation.
and 30øC. Above 35øC the mean water loss increasedmarkedly to 43
percentat 40øC and 93 percentof the body weight per day at 45øC.
Evaporative heat loss.--The percent of the metabolic heat lost by
evaporationwas determinedby dividing the evaporativeheat lossby the
heat produced,which was measuredindirectly by oxygen consumption
(Figure 6). In this calculationit was assumedthat each mg of water
evaporatedremoved 0.58 cal at the body temperature of the bird, and
each cc of oxygenwas equivalentto 4.8 cal. The percentof the heat lost
by evaporation gradually increasedbetween 5ø and 35øC, and sharply
increasedat temperaturesabove 35øC. The increase between 35ø and
45øC was essentiallylinear. At 40øC evaporation accountedfor about
80 percent,and at 45øC, about 125 percentof the heat produced.
Dry heat /low.--Using the sameconversionfactorsas for evaporative
heat loss,the thermal conductanceminusits evaporativeheat component
(C.) was calculated(Figure 7). The methodwas modifiedfrom the one
presentedby Dawson and Schmidt-Nielsen(1966), and the following
equationwasused:
C•) =
M - H.oO
T. -
514
C•^aLES H. TRosr
.5
o
[Auk, Vol. 89
Horned Lark
Dry Conductance
Day
4
4
4
Night
I
!
I
I
I
I
5
10
15
20
25
30
T• øC
Figure 7. The relation of dry heat flow (thermal conductanceminus the evaporative heat loss) to ambient temperature. Symbols, numbers, and symbol displacement
as in Figure 1. The nocturnal valuesare on the right; daytime, left.
where M - H20 is metabolic rate in caloriesminus the caloric equivalent
of the evaporativeheat loss. In order to comparethis calculationwith
Figure 3 the units were reconvertedto cc O.,/g/hr/øC. When calculated
in this manner the differencesbetween the daytime and nocturnal dry
heat flow were reducedbetween 5ø and 25øC, and the zero slope for dry
heat flow was extended to 25øC.
COMPARISON OF MESIC
AND DESERT LARKS
Thermoregulation.--Highambient temperaturesare one of the main
differencesbetweenthe desert and inland valley habitats, at least during
the summer. When exposedto 45øC the desert larks (ammophila) and
the mesiclarks (actia) behaveddifferently (Table 2). The oxygen consumption,and thus heat production,of the desert birds was significantly
lower (P < 0.01) than that of the mesiclarks. The Q•o of the increase
in metabolicrate abovethat at 40øC was 2.4 (TB from 42.5ø to 44.2øC)
in the desertlarks and 3.5 (Tn from 42.5ø to 45.9øC) in the mesiclarks.
The evaporativewater loss in the desert larks was significantly lower
(P < 0.05) than in the mesiclarks.
July 1972]
Horned Lark Adaptationsto Heat
TABLE
515
2
THERM.OREGULATOR¾RESPONSES OF HORNED LARKS FROIV[ MESlC AND DESERT
HABITATS AT AN AMmENT
E. a. actia
(mesic)
•
TEiVIPERATURE Or 45øC
E. a. ammophila
(desert)
Significance
N
SE
,•
N
SE
t
P
3.91
7
0.263
2.97
9
0.117
3.52
< 0.01
45.9
7
0.586
44.2
9
0.208
3.01
< 0.01
103.7
5
3.96
87.6
8
3.48
3.05
< 0.05
1.17
5
0.066
1.32
8
0.028
2.40
< 0.05
Oxygen consumption
(cc O•/g/hr)
Body temperature
(øC)
Evaporative water
loss (% body
wt./day)
EWL/HP
(cal. H.•O/
cal. O0.)
The desert larks did not become as excited when exposedto 45øC
as did the mesiclarks. As a result the desert larks lost a larger portion
of metabolicheat through evaporation(P < 0.05) than did the mesic
larks (abo.ut 132 and 117 percent of the heat produced,respectively).
Correlated
with
the increased heat loss the desert larks maintained
a
body temperaturealmost a degreebelow the ambient temperature,which
the mesiclarks were unable to do. The lowestbody temperatureat which
a bird died from heat stresswas 45.6øC. The body temperatureswere
measured from 15 to 30 minutes after the water loss data were collected.
TABLE
3
WATER CONSUIVIPTION(PER CENT BODY WEIGHT PER DAY)OF HORNED LARKS
FROM MESlC
AND DESERT HABITATS IN RESPONSE TO AMBIENT
oF 23 ø AND 33øC
E. a. actia
(mesic)
TEMPERATURES
E. a. ammophila
(desert)
SE
Significance
•
N
SE
•
N
t
P
28.5
2.5
10
9
7.8
0.6
20.8
2.6
2.3
7
1.0
1.6
10
9
9
2.9
0.4
0.4
0.876
0.138
0.795
>
>
>
0.05
0.05
0.05
Ad libitum tap
Minimum tap
Number of days to
37.1
7.9
9
6
5.5
1.1
50.4
7.1
9
8
8.3
0.7
1.308
0.672
>
>
0.05
0.05
reach minimum
10.3
6
1.7
7.0
8
0.8
1.938 >0.05, <0.10
TA ---- 23øC
Ad libitum tap
Minimum tap
Min. distilled
T.• ---- 33øC
516
C•^RZZS H. T•OSX
[Auk, Vol. 89
This probably explainswhy the mesic larks had an average temperature
of 45.9øC, despite the calculation that they lost about 117 percent of
the heat they produced. The desert and mesic larks were treated in the
same
manner.
Water consumption.--The ad libitum and minimal water consumption
of the desertbirds were not significantlydifferent (P < 0.05) from those
of the mesicat either 23ø or 33øC (Table 3), but the desertlarks were
generallylessvariable, i.e. smaller standard error of the mean, in their
responseto the different drinking regimens. Correlatedwith their more
uniform response,the desert larks required fewer days (P > 0.05, <
0.10) to reach a minimumlevel of water consumptionat 33øC.
Survival without water.•At
the end of the minimum water determina-
tion at 23øC water was removedfrom six larks, and they were weighed
daily until they appearedto be severelystressed(Figure 8). It is interestingthat at least somelarks couldsurvivefor 16 and 31 days without
water. The three desert birds were no better than the three mesic, and
in fact they lostweightmoreconsistently.
Horned
Lark
Weight Losswithout Water
lOO
6•%
...........= Desert
= Mesic
I
I
I
5
10
15
I
20
I
25
I
30
Days without Water
Figure 8. The weight loss per day of three desert (E. a. ammophila) and three
mesic (E. a. actia) Horned Larks without water, but with ad libitum food. The numbers under the lines are the percentagesof the weightson ad libitum water (see text).
Horned Lark Adaptations to Heat
July 19721
TABLE
517
4
CLIMATES O•' TI-IE TWO STIJDY AREAS1
Length Ambienttemperature
øC
of
Population
Station,
elevation
Mesic larks
Warner
(E. a. actia)
record, Mean
years Jan.
Mean
July
Min.
Jan.
Max.
July
Precipitation,
mean annual,
cm
28
6.8
22.8
-11.7
42.8
41.15
28
6.9
27.5
-12.8
44.4
22.61
Springs,
San Diego
County,
California,
969 m
Desert larks
(E. a.
ammophila)
Palmdale,
Los Angeles
County,
California,
787 m
Data from the U.S.
ENVIRONMENT
Weather Bureau, 1964.
MEASUREMENTS
Macroclimates.---AsHorned Larks are open country birds, the macroclimatesof the placeswhere they are found can serve as a useful index
to the environmentalstressesimposed on them (Table 4). Warner
Springs,San Diego County,California,wherethe mesicspecimens
were
taken, has about the samewinter temperaturebut is not as hot in summer as Palmdale,Los AngelesCounty, California, near where the desert
larks were captured. The rainy seasonin both regionsis in the winter,
but Warner Springsreceivesabout twice as muchprecipitationas Palmdale.
Microclimates.--Even though the macroclimatesof open areas are
fairly uniform, the larks do not live in the climates recordedat weather
stationsper se. They selectand to a limited extent create a microclimate
that may be quite different from the macroclimate.Three of their methods of habitat choiceand manipulationare: selectionof cooleror warmer
parts of the habitat duringthe daytime,diggingand useof roostholesat
night, and drinking from man-madewater sources.
Almost daily during the late spring and summer the surface of the
desertfloor becomesvery hot, and at thesetimes the larks rarely alight
on the groundin the sun. They perchin the wind on top of the abundant
creosotebushes,and when they do alight on the ground they fly from
the shadeof one bush to that of another. This is not to say that larks
on the desertare never heat stressed,but they minimizeheat stressby
using the portion of their environmentthat is least stressful. At 12:35
on 18 June 1967 in the Mojave Desert below Red Rock Canyon, Kern
County, California, the temperatureof the groundin the sun was 47øC.
518
Figure 9.
CITARLESH. TROST
[Auk, Vol. 89
A view of a roost hole. Feces can be seenin the bottom.
At a heightof 1.3 m on top of a creosotebushon which a lark had just
beenperchingthe temperaturewas 29.5ø to 31øC, and on the groundin
the shadeof anotherbushto which the lark flew it was 34ø to 39øC, depending on the wind and the amount of sun. This behavioralpattern
has been repeatedlyobservedand appearsto be the commonresponse
of larks to hot environments.
The alpineenvironmentis in generalcold and windy, but on the ground,
particularly in sunny areas, the temperatures can be quite moderate.
Larks were frequently seen resting in the sun in the shelter of rocks or
small bushes.At 2,990 m in Coyote Valley on 12 August 1967, between
11:00 and 15:45 the ground temperaturein such a shelteredspot was
37ø to 39øC. On a nearby rock just 0.3 m higher the temperaturevaried
between24ø and 30øC, and in the shadeit was25ø to 27øC.
A small homeothermsitting exposedin open country on a cold night
is subjectedto considerableheat loss from radiation and convection.
During cold nightsHorned Larks dig roostholesand rest in them (Figure
9). This is apparentlya deviceto reducetheir energylossat night. When
larks wereplacedon a dirt substrateat 10øC in the laboratorythey dug
roostholeswith their bills near the end of their normal photoperiod,but
when kept at 25øC they did not dig roost holes. In the field the larks
frequentlydig the holesbehindprotectivevegetationfrom the prevailing
wind. Larks are usuallythe only birds presentwhere the holesare found
July 1972]
Horned Lark Adaptations to Heat
519
and were often flushed out of them at night. In hard soil, such as near
Warner Springs,the bottom of each hole typically containsfrom 10 to 15
dry bird droppings,whereasthose in the soft soil of the Mojave Desert
usually have only 2 or 3. Apparently larks on soft soil dig new holes
everynight, but in hard soilcountrythey usethe holesfor longerperiods.
The roost holesare just large enough (about 8 X 5 X 4 cm) for a
singlelark to sit in with its back almost level with the ground surface.
In the laboratory three larks placed together in a dirt bottom cage at
10øC dug three separateholes. In the field most of the holesfound were
only large enoughto accomodateone lark, and at one location I found
25 separate holes within a 10-m circle. The only field evidence for
communalhuddling was a group of five holes placed in a 20-cm wide
depression.Perhaps huddling occurs in responseto colder ambient
temperatures. Even a single lark resting in an isolated hole enjoys a
reductionin the amount of exposedsurface area, with a concomitant
reduction
in the radiative
and convective
heat
loss.
If
the
substrate
under the lark becomeswarmer, the heat loss from conductionalso decreases.The roost holeswere associatedwith all the populationsstudied
and appear to be a fine example of how this open country bird adapts
to a rigorousenvironment.
A few larks are scatteredthroughoutthe Mojave Desert, but the population
is densest near man-made
water
sources.
Miller
and Stebbins
(1964) report breedingammophilato be scarcelocal residentsin the dry
drainage sinks of JoshuaTree National park, but in nearby irrigated
areas of the Mojave Desert I found them one of the most abundant birds.
On two trips I made to the irrigated alfalfa fields near Red Rock Canyon
and Palmdale (Kern and Los AngelesCounties,respectively)during the
breeding seasonon 8 June 1967 and 11 June 1968, I found the larks
breedingonly within about 6 km on either side of the irrigated land, although the creosotebush habitat here was indistinguishablefrom that
in the outlying desert. During June the larks did not visit these open
water sources,and presumably made up their water deficits by eating
insects. After the breedingseasonlarge flocks of larks convergeon
water sourcesdaily shortly after dawn. Severalflocks of over 100 larks
flew to poolsof irrigationwater between06:30 and 07:30 on 10 August
1967 in the Antelope Valley west of Palmdale. By 08:00 the incoming
flocks numbered only about 25. The larks usually drank for about 5
minutes and departed,although some larks were present all day. The
flocks consistedof about 60 percent adult and 40 percent young larks
(13 out of 22 capturedwere adults), and are apparentlya post breeding
seasonphenomenon.
520
C•^•zEs H. T•osr
[Auk, Vol. 89
DISCUSSION
Oxygen consumption.--HornedLarks are open country, grounddwellingbirds, and temperatureson the groundin the sun are often high,
even in the alpine environment. The fact that their standard metabolism
is 25 percentlessthan that predictedfor passefinebirds by the equation
of Lasiewskiand Dawson (1967) indicatesa reducedmetaboliccontribution to the total heat load, and shouldbe advantageous
to an animal
in a hot environment(Figure 1). A low metabolicrate has been reported
in severalother birds from hot environments(Bartholomewet al., 1962;
Hudsonand Kimzey, 1966; MacMillen and Trost, 1967a; Lustick, 1968).
The Horned Lark also has a narrow thermoneutralzone at 35øC, probably owing to the low metabolicrate; and in this respectis similar to
the Inca Dove (Scarda/ellainca), another bird from a hot environment
(MacMillen andTrost, 1967a).
At night the larks are quiescent,have a reducedbody temperature,
and the thermoneutral
zone extends downward
to near 20øC.
In
the
field theseenergysavingmechanisms
are probably maximized,as a lark
restingin a roost hole (Figure 9) losesa minimum of heat by radiation
and convection.
The
values for nocturnal
metabolism
obtained
in the
laboratory were gatheredfrom larks sitting on a wire meshin the metabolic chamberand the freely circulatingair doubtlessincreasedheat loss.
The nocturnal oxygen consumptionin thermoneutralityis almost the
sameas that duringthe day at 35øC. The nocturnalratesof many other
birds in thermoneutralityare considerablylower than those during the
day (Benedict and Riddle, 1929; Irving, 1955; Hudson and Kimzey,
1966; Lustick, 1968). At night the larks reach minimal level of oxygen
consumptionwithin 2 hours and maintain it until about 05:00 (Figure
2). After 05:00 the oxygenconsumptionbeginsto rise as the larks appear to anticipate their normal photoperiod (09:00). Birds commonly
showthis anticipationand it probablyoccursin the field (Dawson,1954;
Bartholomew
andCade,1957;MacMillenandTrost, 1967b).
As the daytime metabolicrates below thermoneutralitydo not extrapolate to the observedbody temperature,the larks do not fit the Newtonian coolingmodel as proposedby Scholanderet al. (1950), but the
nocturnalvaluesmorecloselyapproximatethe model. This suggests
that
the daytime metabolicrates are elevated by wakefulnessor alertness,as
Hudson and Kimzey (1966) found in the House Sparrow (Passer
domesticus).
Thermal conductance.--Theconstancyof thermal conductancebetween
5ø and 15øC indicates that temperatureregulation over this range is
maintainedby increasedthermogenesis,
presumablyby shivering(Figure
3). The daytime (0.15 cc O2/g/hr/øC) and nocturnal (0.12) thermal
July 1972]
Horned Lark Adaptations to Heat
521
conductances
are slightly below, but not significantlydifferent from that
predictedby the equationsof Lasiewskiet al. (1967) and Herreid and
Kessel (1967) for a 26-g bird (0.16 and 0.17 cc O2/g/hr/øC, respectively). Between 15ø and 30øC both daytime and nocturnal thermal
conductances
are curvilinear,indicatinga gradual switch from physical
thermoregulationin thermoneutralityto chemical thermogenesis
at low
ambient temperatures.The curvilinear relationship(15ø to 30øC) is
reminiscentof that in the flying fox (Syconycterisaustralis) (Bartholomew et al., 1964) and probably indicates some peripheral heterothermy
and pteromotoractivity over this temperaturerange. The gradualswitch
from physicalto chemicaltemperatureregulationshownby the Horned
Lark has alsobeennotedin severalother passerines
(Dawsonand Totdoff, 1959; West, 1962; Veghte,1964; Lustick,1968).
The influenceof evaporativeheat lossis moreimportantwith reference
to thermal conductance
than one would expectfrom the low and constant
evaporativewater lossbetween 5ø and 35øC (Figure 5). The dry heat
flow (thermal conductanceminus its evaporativeheat component) (Figure 7) is more constantthan thermal conductancebetween 15ø and 25øC.
The higher daytime thermal conductancebetween5ø and 25øC must be
mainly due to increasedevaporativeheat lossduringthe day, for the daytime and nocturnal dry heat flows are similar and there is lesswater loss
at night.
Body temperature.--Horned Larks are excellent homeotherms and
during the day they maintain a constant body temperatureof about
41.5øC over an ambienttemperaturerange of 5ø and 35øC (Figure 4).
This high body temperatureis typical for a small passefine(McNab,
1966). Like most small birds when exposedto ambient temperatureabove
40øC, the larks becomehyperthermic(TB > 42.0øC), whichincreases
the
thermal gradientbetweentheir shell and the environment.They thereby
maximizethe heat lossby radiation,convection,and conductionand thus
reducethe amount of water required for evaporativecooling. Body and
ambient temperaturesare equal when the latter is 45øC, and as this is
near their upper lethal temperature,body temperature is maintained almost solely by evaporativecooling. At night the body temperaturedrops
2.0ø to 2.5øC over an ambient temperaturerange of 5ø to 30øC. A
nocturnaldeclineof this magnitudesavesboth energy and water (MacMillen and Trost, 1967b). This phenomenonhas been known for many
years and is commonin most small birds (Simpsonand Galbraith, 1905;
Baldwin and Kendeigh,1932; Dawson, 1954).
Water loss.--The daytime evaporativewater loss at 25øC (15 percent
of the body weight per day) is almost exactly that Bartholomew and
Cade (1963) predictedfor a 26-g bird (Figure 5). This rate of water
522
CHARLESH. TROST
TABLE
SUMMARY
[Auk, Vol. 89
5
OF DATA ON MINI:M:AL WATER CONSUMPTION OI• S3•ALL BraDS IN Tile
ABSENCE OI• TEMPERATURE
Mean
Species
STRESS
Minimal
water
body wt. % body
(g)
wt./day
Source
Scardafella inca
41.0
8.5
MacMillen and Trost, 1966
Columbinapasserina
Molothrus ater
38.0
33.0
9.7
3.4
Willoughby• 1966
Lustick, 1968
Melopsittacus undulatus
Erernophila alpestris
Carpodacusmexicanus
Passerculussandwichensis
Amphispizabilineata
Taeniopygia castanotis
Sporopipessquamifrons
30.0
26.0
20.6
17.0
13.5
11.5
11.0
(
1.0
1.6-2.6
10.0
26.8-45.9
( 1.0
( 1.0
( 1.0
Cade and Dybas, 1962
Present study
Bartholomew and Cade, 1956
Poulson and Bartholomew, 1962
Smyth and Bartholomew, 1966
Cade et al., 1965
Cade, 1965
loss is considerably above the amount obtained from oxidative water
(Bartholomew and Cade, 1963). During the breeding seasonlarks eat
mainly insects,whereasthey eat seedsthe rest of the year (McAtee, 1905;
Pickwell, 1931). Presumably eating insects during the breeding season
lets them make up their water deficit without visiting open water sources.
At night the water loss is significantlyreduced (7 to 9 percent of the
body weight per day) below that during the day. This 40 to 50 percent
reductionin water loss is advantageousto a diurnal bird that does not
eat or drink during the night (MacMillen and Trost, 1967b). At about
40øC and above the water loss rises sharply as evaporativecoolingbecomesincreasingly important in temperature regulation. More than 100
percent of the heat producedcan be dissipatedby evaporation at 45øC
(Figure 6). This observation
is in agreementwith the findingsof Lasiewski et al. (1966) showingthat all birds they measuredcould lose more
than 100 percent of the metabolicheat by evaporation,when measured
at high TA and low humidities.
Water consumption.--In their water requirementsHorned Larks appear to have better than averagephysiologicalcapacities,but as in their
thermoregulatoryadaptationsthey must rely on a versatile behavioral
repertoire for survival under stressfulconditions. Their ad libitum water
consumptionin the absenceof heat stress (23øC) falls within the expectedrange for a 26-g bird (Bartholomewand Cade, 1963) (Table 3).
A better indication of their adaptation to water shortageis their minimal
water consumptionof 1.6 to 2.6 percent of the body weight per day. Although the Horned Lark requires little water, its minimal water consumptionis intermediatewithin a group of small birds for which these
data are available (Table 5). The Horned Lark has lesseffectivephysi-
July 1972]
HornedLark Adaptationsto Heat
523
ological mechanismsfor water conservationthan several smaller birds.
Both the ad libitum and minimal water consumption
increasewith increasingambienttemperaturein the Horned Lark, as is true of many
otherbirds (Seibert,1949; Dawson,1954; Bartholomew
and Dawson,
1954;Bartholomew
andCade,1956;CadeandDybas,1962;Cadeet al.,
1965;Willoughby,1966). In the field the larks,like otherbirds,compensate for theseincreasedwater demandsby visitingwater sources,eating
insects,and remaininginactivein the shadeduringthe hot part of the
day.
The ad libitum water consumptionof the Horned Lark at both 23ø
and 33øCis greaterthanthe evaporative
waterlossat thosetemperatures
(Table 3, Figure 5). The minimal water requirementsare lessthan the
evaporativewater lossof birds that had beenon ad libitum water prior
to the evaporative
measurements.
Thus larkscan reducetheir evaporative
waterlossunderconditions
of watershortage.
Willoughby (1968) examinedthe water requirementsof two other
alaudidsfromthe NamibDesertin SouthWestAfrica,the 17-g GreybackedFinchLark (Eremopterixverticalis)and the 18.5-g Stark'sLark
(Spizocorysstarki). The Horned Lark utilizesmore water than either
the FinchLark or the Stark'sLark with respectto evaporative
waterloss
(15.0 comparedto 9.6, and 12.0 percentof the body weight per day,
respectively)and with respectto ad libitum water consumption
(20.828.5 versus8.0, and 13.0 percent,respectively). A similar relationship
is shownin the meandaily weightlossof the threespecies
of larks when
deprivedof water; six HornedLarkslost 1.8 percentof the bodyweight
per day, and both the African larks lost less. The Horned Larks did not
appearable to maintainweightindefinitelywithout water, but both the
Africanspecies
could.ApparentlytheseAfricanlarksare physiologically
more specializedfor desert existence,but the Horned Lark is able to
exploitmanydifferenthabitatsovera muchwidergeographic
range.
ComparisonoJ desertand roesiclarks.--In the laboratorythe desert
larks respondin a more uniform manner to stressfulconditionsthan do
the mesiclarks. The water consumption
of the desertand roesiclarks
is not very different,but with the exceptionof ad libitum consumption
at 33øC,the desertlarksconsistently
showlessvariation(smallerstandard
error of the means)than the roesiclarks (Table 3). They alsorequire
slightlylesswateron mostof the drinkingregimens
tested,and require
fewer days to reacha minimallevel of water consumption.The desert
larks are lessvariablein their weight losswithout water and can withstanda slightlygreaterdegreeof dehydration
than the mesiclarks (Figure 8). This greaterdegreeof uniformity,thoughsubtle,may reflecta
more stringentselectionby climate in the desert.
524
Ca^RL•S H. TROST
[Auk, Vol. 89
At ambient temperaturesbelow 45øC the thermoregulatoryresponses
of the two populationsare indistinguishable,
but at 45øC the responses
are very different, and are probablyphysiologicalcorrelatesof behavioral
differences(Table 2). The desert larks apparently do not becomeas
excitedin high ambient temperaturesas the mesiclarks. The desertbirds
evaporatean averageof 18 percentlesswater than those from the roesic
environment at 45øC (87.6 and 103.7 percent of the body weight per
day, respectively),but they also have 32 percent less heat to eliminate
than the roesiclarks (2.97 and 3.91 cc O2/g/hr, respectively).Correlated
with these differencesthe desert larks have a higher EWL/HP ratio,
and thus a lower body temperature. As the lethal T• is only slightly
above45øC, the larks cannotsurvivefurther hyperthermia. The selective
advantagesfor the proper behavioral and physiologicalresponsesat this
critical ambient temperatureare obvious,both with respectto water conservationin an arid environmentand with respectto lethal hyperthermia.
Daytime surface temperaturesin areas inhabited by Horned Larks
are frequently very warm. Although my data are consistentwith the
idea that larks have a low metabolicrate, and thus a reducedmetabolic
contributionto the total heat load in a hot environment,the data do not
negatethe possibilitythat a low metabolismmay also be an adaptation
to food shortage. Lustick (1968) has conclusivelydemonstratedthat the
thermoneutralzoneof a bird can be shiftedto lower ambienttemperatures
with the applicationof exogenousheat. A Horned Lark on the ground
in the sun would probably utilize radiation and extend thermoneutrality
to lower ambient temperatures. In their thermore.gulatoryresponsesto
hot environments,
behavioris just as importantas physiology,and when
the environmentis especiallyhot, such as on the Mojave Desert, larks
select cooler portions of their environment to reduce their heat load
further.
Without transplantationexperiments,or raising animals in the laboratory, it is not possibleto differentiate between genetically and environmentally induced changesbetween populations. Horned Larks are
potentially much more mobile vertebratesthan most mammals, and the
fact that they seemto rely on slight behavioralmodificationsrather than
physiologicaladaptationsmay reflect their relatively recentdispersalonto
such environments as the desert.
AC•C•OWLtDG•E•qTS
This work constitutes a portion of a doctoral dissertation submitted to the Department of Zoology, University of California, Los Angeles, and was supported in
part by NSF Grant G.B.-5139, administeredby G. A. Bartholomew, and by a NIH
Predoctoral Cardiovascular Traineeship (USPHS 5166) under the guidance of J.
Cascarano. Field expenseswere provided by NSF Grant G.B.-3871, to the Departments of Zoology and Botany at UCLA.
July 1972]
Horned Lark Adaptations to Hea•
525
I wish to give specialthanks to G. A. Bartholomew for guidance,criticism,material
goods,and advice. R. C. Lasiewski and J. H. Brown provided stimulating discussion
and criticism. S. Lustick helped in thought and field. Finally, I especially wish to
thank my wife, Lucille M. Trost, who helped make this study possible.
SUMMARY
The behavioral and physiologicaladaptationsof two subspeciesof
Horned Larks are examined and compared. The larks are a desert form
(Eremophilaalpestrisammophila)from the hot and dry Mojave desert
and a more mesic form (E. a. actia) from the relatively mild inland
valleys of California.
Horned Larks have a low standardmetabolicrate (2.28 cc O2/g/hr)
and a high thermoneutralzone (ca. 35øC), both of which indicate the
larks are well adaptedto a warm, open environment.At night the larks
have a 2.0ø to 2.5øC drop in body temperature,their metabolicrate is
reduced,thermoneutralityis extendedto near 20øC, and their evaporative
water loss is about half the daytime level. All these energy and water
saving mechanismsare beneficial to a diurnal bird that does not eat or
drink at night. In the field at night behaviorsupplements
physiology
when larks selector create a microclimatein a roost hole, which undoubtedlyis not sostressfulas the macroclimate.
The water requirementsof Horned Larks are not exceptionallylow
for smallbirds, and the larks must rely on a versatilebehavioralrepertoire
for survival under stressfulconditions. The temperature regulation at
high ambienttemperaturesof desertlarks is superiorto that of larks from
a more mesic environment,and is probably a physiologicalcorrelate of
behavioraldifferences.The apparentrelianceon behavioral,rather than
on physiologicaladaptationsis probably a reflection of the recent dispersal of the larks onto the desert.
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